Behavioral Ecology Advance Access originally published online on March 9, 2005
Behavioral Ecology 2005 16(3):624-633; doi:10.1093/beheco/ari037
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Allometry and variability of resource allocation to reproduction in a wild reindeer population
a UMR-CNRS 5558, Laboratoire de Biométrie et d'Ecologie Evolutive, Université Lyon 1, 69622 Villeurbanne cedex, France, and b Norwegian Institute for Nature Research, Tungasletta 2, 7485 Trondheim, Norway
Address correspondence to A. Loison. E-mail: loison{at}biomserv.univ-lyon1.fr.
Received 17 November 2003; revised 13 January 2005; accepted 23 January 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSTUDY AREA AND POPULATIONANALYSISRESULTSDISCUSSIONREFERENCES |
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The differential allocation of energy to either reproduction or survival represents a major conflict with important implications for patterns of life history. Here, we explore how covariation between maternal body weight and fetal weight vary according to fetal sex in a wild reindeer (Rangifer tarandus) population during two contrasting years. Maternal weights differed during the 2 years, probably because of a difference in population density. We could not detect any change in the allocation to reproduction depending on female phenotypic distribution. Male fetuses were heavier than female fetuses, with the same relative dimorphism in both years. There was no support for a correlation between the sex of the fetus carried by a female and her weight. Our results suggest that the level of resource allocation to reproduction during the prenatal period is strongly determined by female body weight and the allometric relationship between body weight and metabolic rate. We discuss the consequences of our results for population dynamics. We call for an integration of inter- and intraspecific allometric approaches to better understand constraints and variation in life-history traits.
Key words: allometry, body weight, prenatal resource allocation, Rangifer, reindeer, sex bias.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSTUDY AREA AND POPULATIONANALYSISRESULTSDISCUSSIONREFERENCES |
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The trade-off between reproduction and survival is a core-concept of life-history strategies (Stearns, 1992
). The diversity of life-history strategies can be structured along a main axis, the body weight axis, which accounts for the allometric component of life-history strategies (Calder, 1984). This axis explains up to 50% of the variation of ecological life-history traits (Peters, 1983; Western, 1979) and up to 75% of the variation of physiological traits (Calder, 1984). Among homeotherms for example, species body weight is generally a good proxy of the strategy of resource allocation towards reproduction per breeding attempt (Allainé et al., 1987; Clutton-Brock, 1991; Sæther, 1985; Webb, 1997). In mammals, especially when accounting for phylogeny (Stearns, 1983, 1992), the level of allocation to reproduction, measured as litter weight relative to adult female weight, is relatively well predicted by species mean body weight (Martin and MacLarnon, 1985; Millar, 1981; Reiss, 1989). The increase in litter weight with female body weight is however not isometric and larger species tend to invest relatively less in their offspring per breeding attempt than smaller species (Clutton-Brock, 1991; Pontier et al., 1993), following the pervasive negative allometric relationship found between body weight and physiological traits (Calder, 1984; Kleber, 1961; Martin, 1988; Robbins CT and Robbins BL, 1979).
This negative correlation between maternal body weight and the relative level of energy allocation per breeding attempt is well established at the interspecific level by studies of static interspecific allometry (sensu Martin, 1988), that is, studies comparing life-history traits among species. The focus of population studies is usually quite different as they aim at disentangling the relationships between individual traits and fitness under varying environmental conditions. Body weight is used as a proxy for individual quality as most empirical studies demonstrate strong covariation of body weight with most life-history traits (e.g., Albon et al., 1983; Brown, 1983; Festa-Bianchet et al., 1997; Gaillard et al., 2000a; Genoud and Perrin, 1994; Mysterud et al., 2001; Sedinger et al., 1995; Wikelski and Romero, 2003). The possible allometric relationship between individual body weight and life-history traits is most often overlooked (i.e., the static adult allometry approach, sensu Martin, 1988), with the exception of few studies of invertebrate species and fishes (see Reiss, 1989, for a review).
These contrasted approaches at the inter- and intraspecific levels would benefit from being reunified to provide insights into the tactics of energy allocation (Begon et al., 1996). Indeed, it is not clear from existing studies whether resource allocation tactics towards reproduction are fixed within a given species or whether individuals within a population or among populations are able to modify their allocation tactics depending on their own or environmental conditions. Several studies show that when individuals vary in size or condition during their lifetime, their reproductive output also varies (Clutton-Brock, 1991, and see e.g., Mauck and Grubb, 1995, in birds; Jordan and Snell, 2002, in lizards; Siems and Sikes, 1998, in fishes; Arnborn et al., 1993; Bowen et al., 2001, in pinnipeds; Festa-Bianchet and Jorgenson, 1998, in ungulates). However, the positive covariation between mother and offspring weight alone would not demonstrate a change in the resource allocation tactics if this variation followed the same allometric axis (Figure 1a) constrained by the species life-history strategy and physiology (Begon et al., 1996). Unfortunately, it is often not possible to deduce from empirical studies at the population level whether the reported variation in offspring body weight when female phenotype or environmental condition change truly reveals variation in the allocation tactic, that is, a change in the slope or intercept of the allometric relationship between female and offspring body weight (e.g., such as in Figure 1b–d). Indeed, the allometric exponent of the relationship between body weight and reproductive output is rarely measured despite the insight it might provide on the possible mechanisms or constraints underlying resource allocation tactics.
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Here, we will test whether the sex-specific level of energy allocation to reproduction was modified at the intraspecific level after a change in the phenotypic condition of females in a wild population of a large mammal, the wild mountain reindeer (Rangifer tarandus). This population (in Hardangervidda National Park, Norway) has been monitored over a long period (1954 to present) and has undergone several dramatic changes in densities (Skogland, 1990
). These fluctuations in density have been shown to affect birth weight, age at maturity, juvenile survival, and adult body weight, all measured from harvested individuals (Skogland, 1986, 1990). It was therefore an appropriate setting to focus on how these large fluctuations would affect the level of resources allocated by females to reproduction.
We first examined three alternative hypotheses predicting how maternal resource allocation should vary according to the female phenotype. The first hypothesis corresponds to the null hypothesis (H0) stating that the level of resource allocation to reproduction should not change within a population of a given species, even when female phenotype or environmental condition changes (P1 in Table 1, Figure 1a). The second hypothesis (P2 in Table 1, Figure 1b) corresponds to one of the alternative hypothesis to H0, whereby females may favor their own maintenance over investment in their offspring when conditions deteriorate. This alternative generalizes the idea that females can adopt "selfish" strategies (sensu Festa-Bianchet and Jorgenson, 1998) when encountering unfavorable environmental conditions. In contrast, the third hypothesis (P3 in Table 1, Figure 1c) assumes an increase in the allocation to reproduction when females are facing poor conditions. This hypothesis follows Skogland (1989, 1990), who specifically proposed that natural selection could lead to an "increased reproductive effort by smaller females when food was limiting" (p. 442). Indeed, if low female body weights resulted from an increase in density and/or age-specific selective pressure against large-size individuals, we could expect that females allocated more of their resources into reproduction for a given body weight when the average female weight is low, in agreement with results previously found in heavily exploited fish species (Reznick and Ghalembor, 2001; Reznick et al., 2001; Rochet et al., 2000). By studying the relationship between offspring and mother weights, we could also test whether this relationship was isometric (hypothesis P4, Table 1) or similar to the allometric relationship expected at the interspecific level (hypothesis P5, Table 1), that is, with an allometric exponent of 0.75 (Millar, 1981; Robbins CT and Robbins BL, 1979).
Then, we focused more closely on possible changes in the sex-specific resource allocation by fetus sex, after the change in phenotype among females (Andersson, 1994; Leblanc et al., 2001). Modification of the sex of the offspring or of the sex-specific allocation make sense under the condition of sexual dimorphism in offspring size, which is the case in reindeer (Kojola, 1993; Krebs and Cowan, 1962; Rönnegård et al., 2002). Male-biased resource allocation and sexual dimorphism should be greater when resources are abundant and do not potentially limit to the mother's ability to provide for the energetic demands of male offspring (Pélabon et al., 1995). In addition, the ability of relatively large females to produce an excess of males in polygynous ungulates, as expected according to the Trivers and Willard (1973) model of adaptive sex ratio (Cameron, 2004; Hewison and Gaillard, 1999), may only occur when females are in a good condition (e.g., Kruuk et al., 1999, in red deer; see Cameron, 2004, for a review). We therefore tested a final series of three predictions. First (P6, Table 1), given the size dimorphism at birth between male and female reindeer calves, the absolute difference between sexes in fetus weight should be lower at low average female weight than at high female body weight (see Leblanc et al., 2001, in bighorn sheep). Second (P7, Table 1), the relative difference in weight between male and female fetuses should also be larger when average female body weight is low as fetus growth in males should be more affected by resource restriction than females (Clutton-Brock et al., 1985; Loison et al., 2004). Finally (P8, Table 1), we expected a relationship between maternal weight or condition and the sex of the fetus to be more likely to occur when the average condition of females is good, as found by Kruuk et al. (1999) in red deer.
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STUDY AREA AND POPULATION |
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TOPABSTRACTINTRODUCTIONSTUDY AREA AND POPULATIONANALYSISRESULTSDISCUSSIONREFERENCES |
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The study population is located in the Hardangervidda National Park in Norway, a high mountain plateau of approximately 8200 km2 entirely above the tree line, consisting of alpine tundra habitat. A more detailed description of the study area and the reindeer population can be found in Skogland (1984a)
. The population size has fluctuated widely between approximately 9000 and 35,000 animals during the last 30 years (Skogland, 1990). During the years of peak abundance (Figure 2), reindeer demographic parameters have exhibited clear signs of density dependence, with lower reproductive performance and lighter body weight (Skogland, 1989, 1990). To restore overgrazed lichen dominated winter pastures, which constitute the main forage for reindeer during winter, managers decided to reduce the population by more than 50% in two successive years in 1983 and 1984. Since then, harvesting quotas have been set to maintain a winter population at or below 10,000 animals. As part of the management plan for the population, annual minimum counts are conducted using airplanes (more details in Skogland, 1990). The quotas fluctuated between 2500 and 11,000 reindeer during the 1985–2000 period. The success of hunters in killing animals varies greatly between years, and a relatively small proportion of the prescribed quota is ever killed. The number of killed and removed animals has thus varied between 751 and 4400 during this period (Figure 2).
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In 1983 (a peak density year) and 1997 (a low-density year), a small proportion of the reindeer quota was allocated to scientific research, with the possibility of hunting reindeer during winter. Accordingly, 71 female reindeer (60 being pregnant) were harvested in 1983 and 79 female reindeer (71 being pregnant) in 1997. The culling occurred during three periods, one in early February, one in mid-March, and one in mid-April. As the rut occurs during late September and October in the Hardangervidda population (Skogland, 1990
), these periods corresponded to fetuses aged approximately 5, 6, and 7 months, respectively. Dressed body weight was measured after removal of the skin, head, guts, and hoofs and is referred to as body weight. Fetuses were sexed and weighed to the nearest 10 g. |
ANALYSIS |
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TOPABSTRACTINTRODUCTIONSTUDY AREA AND POPULATIONANALYSISRESULTSDISCUSSIONREFERENCES |
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We analyzed three main variables: maternal body weight, fetal body weight, and fetus sex ratio. We used linear models (analysis of covariance [ANCOVAs]) for the three first variables and logistic-linear models (logistic ANCOVAs) for the sex ratio. We only considered pregnant females
2 years of age as we were interested in reproductively active females. Females pregnant when aged 1 year were found in 1983 (five of the 6 1-year-old females harvested were pregnant, see also Skogland, 1990), while no 1-year-old female was harvested in 1997. We therefore tested for difference in absolute and relative prenatal care between 1983 and 1997 only with females 2 years of age.
Analyses of female body weight
Our first aim was to demonstrate that the distribution in maternal body weight and condition was indeed different during the two study periods. To compare years, we first had to account for age and date of killing (Julian dates). Age was determined from the number of layers in the secondary dentine of the incisors in adults (Nordby, 1968). We modeled the effect of female age either through a quadratic relationship, with three age-class categories (young females: 2 years of age; prime-age females: 3 to 9 years of age; old females: >9 years of age) or two age-class categories (young females: 2 years of age; adult females: 3 years of age). These age-classes were based on the results from previous studies showing that young, often first-time breeders and old females have lighter calves than prime-age females (Rönnegård et al., 2002; Thomas et al., 1989; Weladji et al., 2002). We then calculated the adjusted female body weight to the 20th of March, which was the mean date of sampling. The adjusted body weight was log transformed to allow analysis of the weight of fetuses proportional to weight of the females (see below).
Analyses of fetus body weight
Fetal body weights were analyzed according to year, date, sex, and maternal body weight. We log transformed the fetus body weight to account for fetus growth that is not linear during the gestation period (Gaillard et al., 1997a; Robbins CT and Robbins BL, 1979). To explore the relationships between fetal body weight and maternal weight, we calculated the residuals of the model selected for explaining variation in maternal weight, which we designated as relative maternal weight. This relative maternal weight corresponds to a measure of whether females were heavier or lighter than the mean females of their age and year of harvest, accounting for the date of culling.
To further investigate the relative energy allocation to reproduction and more specifically the allometric relationship between fetal weight and maternal weight, we regressed the log-transformed fetal weight against the log-transformed maternal weight. We adjusted the fetal and the maternal weights to the 20th of March (mean date of sampling). The test of whether fetal weight increased with the same slope and intercept relative to maternal body weight in each year was conducted by testing for the interaction between year and mother weight. We also compared the slope of the regression to 1 (hypothesis of an isometric relationship) and to 0.75 (hypothesis of a negative allometric relationship like the interspecific relationship, Kleber, 1961; Robbins CT and Robbins BL, 1979).
Analyses of fetal sex ratio
We examined whether the sex ratio (defined as the probability of producing a male) depended on date, year, and maternal body weight. Note that when sex ratio is defined at the individual level as the probability of producing a male, it corresponds at the population level to the ratio of the number of males to the total number of males plus females. We only used the residual maternal weight as we were interested in whether relatively heavier females preferentially produced male fetuses. We checked the interaction between year and maternal body weight to test whether the relationship between sex ratio and maternal body weight differed in 1983 and 1997. Testing for the date effect on sex ratio allowed us to test for the possibility that differential mortality of the fetuses could induce a biased sex ratio (Cameron et al., 1999; Forchhammer, 2000; Kruuk et al., 1999; Myers, 1978; Mysterud et al., 2000).
All analyses were performed with S-PLUS (Venables and Ripley, 1999). Mean estimates are given ± standard errors. When we had more than four variables in the models, we selected the model using the Akaike information criterion (Burnham and Anderson, 1998; Venables and Ripley, 1999), which allows selection of the "best" models among a set of models, according to the parsimony principle (see Johnson and Omland, 2004, for a recent review on criterion-based model selection).
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RESULTS |
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TOPABSTRACTINTRODUCTIONSTUDY AREA AND POPULATIONANALYSISRESULTSDISCUSSIONREFERENCES |
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Female body weight
We tested for differences in maternal body weight between the two study years by analyzing female weight with respect to age-class, date, and year, which were all included in an ANCOVA. The best model comprised all the main terms plus the interaction terms between date and age-classes and between date and year (Table 2). Young females weighed consistently less than prime-age females, but the interaction between date and age-classes revealed that this difference increased with harvesting date (average difference at the mid-date of culling: 1.63 kg ± 0.83; no difference in early February, up to 3.6 kg difference in mid-March). Indeed, young females were lighter when harvested late in the winter (weight loss in 1983: –0.079 ± 0.030 g per day; in 1997: –0.043 ± 0.030 g per day), while the mean weight of adult females remained fairly constant with harvesting date (weight loss in 1983: –0.016 ± 0.017 g per day, t = –0.92, p = .36; in 1997: 0.020 ± 0.015 g per day, t = 1.31, p = .19). The year effect indicated that females were lighter in 1983 than in 1997 (Table 2). Prime-age females were constantly heavier in 1997 than in 1983, with a mean difference of 4.72 kg ± 0.54 (weight adjusted to the 20th of February, Figure 3). The interaction between year and date denoted a different effect of harvesting date between years, with a sharper decline in average weight in 1983 than in 1997 for young females (but not for adult ones, see values above). Modeling age effect using a second-order polynom or three age-classes did not improve the model as body weight hardly decreased with age: the mean difference in weight between prime-age and old females at the mid-date of culling was 0.41 kg ± 0.93 (t = –0.44, p = .66) in favor of prime-age females.
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AIC)
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Fetus body weight
We tested whether fetal weight (predictions P1–P5, Table 1) and size dimorphism (predictions P6 and P7, Table 1) in fetal weight were larger when females were heavier. We therefore analyzed fetal body weight (log transformed) in an ANCOVA with culling date and relative maternal body weight as covariates and year and sex as factors. Fetal body weight differed by culling date, year, sex, and the relative maternal body weight, with a significant interaction between date and year (F1,109 = 4.85, p = .03; all other four-way, three-way and two-way interactions were nonsignificant with p > .15). This interaction between date and year demonstrated that fetuses had grown more rapidly in 1997 (b = 0.026 ± 0.001) than in 1983 (b = 0.022 ± 0.001, Figure 4) in both sexes. Therefore, male and female fetuses were larger for any given date in 1997 than in 1983. The sex effect confirmed a sexual dimorphism in fetal body weight during pregnancy in reindeer (difference of 0.099 ± 0.038 on the log scale in favor of male fetuses, Figure 4). Because fetuses of both sexes were larger in 1997 than in 1983, but without any significant interactions between date and sex (F1,123 = 0.05, p = .82) or year and sex (F1,123 = 0.06, p = .80) on the log scale, we could conclude that the absolute difference in weight between male and female fetuses was larger in 1997 than in 1983 (supporting prediction P4, Table 1) but that the relative dimorphism was similar in both years (rejecting prediction P5, Table 1). Relative maternal body weight was positively correlated to fetus weight (b = 0.024 ± 0.007) and had the same effect in both years (nonsignificant interaction between relative maternal weight and year: F1,108 = 0.46, p = .49).
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To explore whether the relative investment in the fetus differed between years (predictions P1–P3, Table 1), we performed analyses with log-transformed fetal and log-transformed maternal weights, both adjusted to the 20th of March. Fetal weight increased with the same slope (i.e., allometric exponent) and the same intercept in both years and for both sexes (main effect: F1,111 = 1.03, p = .31; interaction with adjusted female weight: F1,110 = 0.74, p = .39; interaction with sex: F1,110 = 0.02, p = .89). We therefore could not reject the hypothesis of a lack of modification in the tactic of resource allocation (P1, Figure 1a) and our results gave no support to the alternative hypotheses (P2 or P3, Table 1; Figure 1b,c). The best model only included the main effects of fetus sex and adjusted maternal weight (F1,112 = 6.63, p = .01 and F1,112 = 29.46, p < .01, respectively), while none of the two- and three-way interaction terms were significant (all p values >.40). The allometric exponent was 0.740 ± 0.136 (Figure 5), which was not significantly different from 0.75 (Z = 0.07, p = .94) but significantly different from 1 (Z = 1.91, p = .05). The difference between sexes only impacted the intercept with a difference of 0.100 ± 0.037 in favor of males. Although nonsignificant, the year effect indicated that fetuses were slightly heavier for a given adjusted maternal weight in 1997 than in 1983 (b = 0.118 ± 0.332).
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Fetus sex ratio
We found no evidence of a sex-biased mortality of fetuses in utero during winter and no evidence of a difference in the overall sex ratio during the 2 years. Indeed, the probability of producing a male did not vary with year or date (interaction:
2 = 0.132, df = 1, p = .72; main effect of year: 2 = 0.11, p = .74, main effect of date: 2 = 0.04, df = 1, p = .84). The mean sex ratio (number of male fetuses divided by the total number of fetuses) was 0.45 ± 0.06 in 1983 and 0.48 ± 0.06 in 1997.
The effect of maternal weight on sex ratio differed in 1997 and 1983 (interaction between relative maternal body weight and year: 2 = 5.13, df = 1, p = .02). In 1997, relatively larger females tended to preferentially have female fetuses (slope of the logistic relationship: –0.199 ± 0.098), while no significant relationship occurred in 1983 (slope: 0.326 ± 0.398). Age effect modeled as a category or as a second-order polynom was not significant, neither in the three-way interaction between age, year, and residual female weight (2 = 1.97, df = 2, p = .37, model with age as a polynom), nor in any two-way interactions (age with year: 2 = 0.44, df = 2, p = .82; age with residual body weight: 2 = 0.35, df = 2, p = .17), or as a main effect (2 = 0.23, df = 2, p = .89).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSTUDY AREA AND POPULATIONANALYSISRESULTSDISCUSSIONREFERENCES |
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We have shown that the resource allocation to reproduction was mostly determined by maternal weight and fetal sex, with similar patterns observed in the two samples, despite differences in female body weight. At the intraspecific level, we demonstrated that the allometric exponent of the relationship between female weight and fetus weight was strikingly close to 0.75, the value usually found at the interspecific level for life-history traits related to the metabolic rate (Kleber, 1961
; Robbins CT and Robbins BL, 1979). Our results thus indicate that female resource allocation to reproduction may be strongly constrained by physiology at the intraspecific level. That male fetuses were not proportionally heavier than female fetuses when females were heavier also supports the conclusion that there is a lack of variation in the tactics associated with resource allocation. We discuss below (1) the extent of the difference in the distribution of female phenotypes; (2) the variation in the resource allocation to reproduction and allometry patterns expected at the individual, population, and species levels; (3) the sex-specific resource allocation to reproduction; and (4) the possible consequences on the population dynamics of the lack of short-term variation in resource allocation to reproduction.
Variation in female phenotypes
The series of hypotheses we tested (Table 1) depended on the females having different phenotypes (i.e., body weights) in the two different sampling years. Indeed, a response of life-history traits is only expected under some modification of the selective pressure encountered by individuals in the short and/or long term (Reznick and Ghalembor, 2001; Stearns, 1992; Zera and Harshman, 2001). The difference in body weight highlighted here was quite striking. Indeed, because carcass weight is about 50% of the live weight (Strand, unpublished data), the difference of more than 4.7 kg on mean female carcass weight would translate into a difference of about 9.4 kg of live weight. Interestingly, this is greater than the amplitude of year-to-year variation in average female carcass weight reported for natural populations of reindeer in similar environments during consecutive years, which is less than 3 kg (populations under experimental supplemental feeding excluded; Helle and Kojola, 1993). We could therefore reliably conclude that these 2 years were representative of two periods during which the average population phenotype differed, independently of year-to-year variations affecting any individual female during her lifetime (e.g., Festa-Bianchet and Jorgenson, 1998, in bighorn sheep; Gaillard et al., 2000a, in roe deer). Because these years were separated by 14 years, this also ensured that sampled females did not share similar environmental conditions during their lifetime.
The causes of this large difference in female average body weight can be sought in differences in density and in climate. The early winter harshness can greatly influence the body mass of ungulates during winter (e.g., Loison et al., 1999, in red deer). However, the average snow depth between November and March was similar in 1983 (92 cm) and 1997 (95 cm), given that the average between 1975 and 2000 was 70 cm (range: 17–139 cm). It seems therefore unlikely that snow depth would account for the amplitude of the difference in body weight between 1997 and 1983. Previous studies have attributed variation in body weight in this and other reindeer populations (Skogland, 1989, 1990) to differences in population density relative to the availability of summer forage (Helle and Kojola, 1993; Reimers, 1997; Reimers et al., 1983). The population on Hardangervidda was undergoing a high-density period in 1983 during which the lichen was recognized to be in a bad condition (Skogland, 1984b, 1988) and a low-density period in 1997, after intense harvesting aimed at both reducing the reindeer numbers and improving the state of lichens (Figure 2). It is therefore likely that the difference in density is the main cause of the difference in female weight between 1983 and 1997. A strong negative impact of density on adult body weight is a common result among large mammals (review in Fowler, 1987; Sæther, 1997; and for examples in ungulates, see e.g., in red deer: Mysterud et al., 2001; roe deer: Gaillard et al., 1996, Vincent et al., 1995; bighorn sheep: Festa-Bianchet et al., 1998; Jorgenson et al., 1993; Leblanc et al., 2001) and is pervasively reported in reindeer (Helle and Kojola, 1993, 1994; Reimers et al., 1983; Skogland, 1990). The important assumption that the distribution of female phenotypes differed beyond year-to-year variation in body weight during the 2 years of study was reasonable, allowing the set of hypotheses presented in the introduction to be tested.
Allometry in resource allocation to reproduction
The contradiction often pointed out (e.g., Boyce, 1989) that the correlation between body weight and relative offspring weight is negative at the interspecific level and positive at the intraspecific level may partly come from methodological misunderstandings. At the intraspecific level, the body weight of the litter/clutch is often explained by the maternal body weight using a regression without log transforming the data (Festa-Bianchet et al., 1998; Jordan and Snell, 2002; Keech et al., 2000; Loison et al., 2004; Wikelski and Romero, 2003). The slope of this regression is tested for a significant difference with 0 as the null hypothesis is the lack of relationship between female weight and offspring weight. At the interspecific level, the regression performed between these two variables always relies on a log transformation of the weights (LaBarbera, 1989), and the null hypothesis is that the slope is different from 1 (i.e., an isometric relationship). Negative allometric exponent (i.e., slopes smaller than 1, Martin, 1988) are pervasively found when comparing female weight and offspring weight (Martin and MacLarnon, 1988; Sæther, 1985) and reveal that the relative offspring weight decreases with increasing female weight. Here, we showed that the relationship between maternal weight and fetal weight was allometric at the intraspecific level as well, with an exponent congruent with the one found at the interspecific level among ungulates (Martin and MacLarnon, 1988; Robbins CT and Robbins BL, 1979). We therefore found no discrepancy between inter- and intraspecific patterns. The value of the negative allometric exponent we estimated (0.74) strongly suggests that prenatal allocation to reproduction was constrained by female metabolic rate. This may be particularly pronounced because we were focusing on resource allocation during the prenatal period only and studying a monotocous mammal. At this stage, behavior, experience, and heterogeneity in female quality may be less influential in determining the weight and growth of the fetus than they are on the growth of the offspring after birth (e.g., Bowen et al., 2001; Cameron et al., 2000; Clutton-Brock, 1984, 1988, 1991; Genoud and Perrin, 1994; Loison et al., 2004).
The relationship between maternal weight and fetal weight was similar during the two contrasted periods not only because the slope of the allometric regression did not differ but also because we could not detect any difference in the intercept (see Figure 1a). Nonsignificant results always raise the question of a possible lack of power in the statistical analyses (Steidl et al., 1997). However, the size of the data set was reasonably large for a study of a large mammal population, and all samples were collected within an experimental setting, ensuring precise measurements. We can therefore be confident that there were no large differences in the level of resource allocation to reproduction during the two periods.
The hypothesis of an increased resource allocation strategy when females were lighter (P3 in Table 1, Figure 1c) was based on the Skogland (1989, 1990) hypothesis that the age-specific selective pressure due to hunting had changed enough in this population to induce changes in reproductive life-history traits. Such patterns were indeed highlighted by Reznick and Yang (1993) on guppies and Rochet et al. (2000) in several fish species (see also Reznick and Ghalambor, 2001, for a review of empirical studies). We cannot discriminate from the data alone whether the lack of increase in resource allocation to reproduction was due to a too small change in the age-specific selective pressure and/or to a species-specific fixed level of resource allocation to reproduction. The high- and low-density periods may not have been long enough compared to the generation time of reindeer (up to 12 years, Gaillard, 1991) to lead to a change in prenatal resource allocation to reproduction, especially because this life-history trait is strongly related to physiology in mammals (Martin and MacLarnon, 1988; Millar, 1981). The recent review by Reznick and Ghalembor (2001) exemplifies that life-history traits values only shift within the contemporary time scale under dramatic changes in their environmental conditions and age-specific selection pressure. However, as discussed above, resource allocation tactics may be strongly constrained by physiological processes during the prenatal period (Robbins CT and Robbins BL, 1979). The problem of disentangling the consequences of allometric energetic constraints from different ecological conditions is often overlooked. Studying the combination of physiology, energetics, and life history at both the intra- and interspecific levels would however shed interesting light on the possible range of interindividual variation in resource allocation tactics (Begon et al., 1996; Martin, 1988; Zera and Harshman, 2001, and see Brown, 1983, for an empirical example).
We did not find support for the hypothesis of a selfish tactic among females (Figure 1b), such as the one highlighted by Festa-Bianchet and Jorgenson (1998) for bighorn sheep. This hypothesis relies on the idea that females of iteroparous species could invest less in reproduction when in bad condition, thereby enhancing the chance of successfully reproducing if density or environmental conditions were to improve (e.g., Festa-Bianchet and Jorgenson, 1998; Mauck and Grubb, 1995). However, such a tactic has been shown at the individual level, while, as shown on Figure 1d, within-individual variation in the allocation to reproduction does not imply any response at the population level. We could only rule out such a response at the population level, but we have no information about the temporal variation in individual tactics in our population as it would require the monitoring of individually known animals in the long term. Unfortunately, few studies allow monitoring year-to-year changes in body weight of females and of their consecutive offspring in wild populations (Festa-Bianchet and Jorgenson, 1998).
Sex-specific resource allocation
As expected for reindeer (Kojola, 1993; Krebs and Cowan, 1962; Rönnegård et al., 2002), we highlighted different levels of resource allocation to male and female fetuses. Male fetuses were more costly to produce as they were heavier and grew faster than female fetuses, in agreement with previous studies of sexual dimorphism in reindeer birth weight (Kojola, 1993; Krebs and Cowan, 1962; Rönnegård et al., 2002; Weladji et al., 2003). The absolute difference between male and female fetuses was larger when the females were heavy on average (see also Leblanc et al., 2001, for bighorn sheep), but the proportional difference was not, as disclosed by our analysis on the log scale. The hypothesis that offspring dimorphism is constrained by the total energy available for the mother (Byers and Hogg, 1995; Byers and Moodie, 1990) was not supported by our results (see Pélabon et al., 1995, for a detailed discussion of this hypothesis). This suggests that there was no important change in the tactic of sex-specific resource allocation depending on female phenotype.
The sex ratio (proportion of males) of sampled fetuses was similar during the 2 years. This was expected because the adjustment of sex ratio depending on maternal condition (Trivers and Willard, 1973) should occur at the individual and not at the population level (Hewison and Gaillard, 1999). However, even at the individual level, our results did not support the Trivers and Willard (1973) model, which predicts that larger females should preferentially produce males in polygynous ungulates for which the assumptions of their models are fulfilled (Hewison and Gaillard, 1999). Reindeer, like red deer (Kruuk et al., 1999), should be among those (see more details in Hewison and Gaillard, 1999), although results in reindeer have not consistently supported the Trivers and Willard model (no sex bias according to maternal condition: Kojola, 1993, Kojola and Helle, 1994, Reimers and Lenvik, 1997, Thomas et al., 1989, Weladji et al., 2003; male-biased sex ratio with increasing maternal condition: Cameron et al., 1999; Kojola and Eloranta, 1989). A refinement of the model has been proposed by Kruuk et al. (1999) in red deer, who demonstrated that the expected sex bias was apparent at low density only (see also Weladji and Holand, 2003, in reindeer). Our results challenged these expected patterns. However, the Trivers and Willard model relies on a relationship between fetus sex and maternal condition at conception (Cameron, 2004), while we studied maternal weight during gestation. Whether there is an adaptive manipulation of the sex ratio at conception depending on the maternal condition is therefore difficult to evaluate with our data set as the sex-specific energetic costs of fetuses may lead females carrying a male fetus to loose more weight during gestation than females carrying a female fetus. Several alternative hypotheses can also explain a lack of support of the Trivers and Willard (1973) model based on a questioning of the basic hypotheses on which it relies. For example, even in polygynous species, females may have a larger impact on the reproductive success of their daughters than of their sons (Cameron, 2004; Clutton-Brock and Vincent, 1991; Dittus, 1998; Emlen, 1997) when the quality and reproductive success of sons is determined by events occurring after independence. Dominance rank or home range of daughters and not of sons can be influenced by maternal traits (Byers, 1997). More detailed studies on the impact of female care on their daughter's reproductive success are badly needed in reindeer. More generally, there is a need for better evaluations of the assumptions of the Trivers and Willard model (Hewison and Gaillard, 1999), for longer monitoring of the relationship between individual female condition and the reproductive success of their offspring (Brown, 2001) and for a use of more appropriate measures of female conditions at the time of conception (Cameron, 2004).
Consequences of resource allocation tactics for population dynamics
In most mammals, birth weight and birth date greatly influence the survival of offspring (Andersen and Linnell, 1997; Boltnev et al., 1997; Chambellant et al., 2003; Clutton-Brock et al., 1987; Gaillard et al., 1997b). The comparison of 2 years with contrasting maternal weights clearly showed that for any given date, fetuses were lighter when the average female weight was low. The difference in fetal weight at a given date could have resulted from fetuses being of different ages. Indeed, delayed dates of conception can appear at high density (Clutton-Brock et al., 1982), for example, if the condition of females limits their possibility to enter early into estrus. Skogland (1990) reported an 8-day delay in the birth peak in 1983 (high density) compared to 1989 (after the decrease in density) in our study population. However, if the difference in fetal weight was only a matter of age, we would have found similar fetus growth rates. Instead, we found a higher growth rate when the average maternal weight was high; therefore, delayed conception alone cannot account for the differences in fetal weight. In addition, lower fetal weight for a given date and lower growth rate may not be completely compensated for by a longer gestation date, so that we can expect birth weights to have differed between the 2 years. Because there was no shift upwards in the prenatal resource allocation to reproduction when females were light, the direct consequence of a lower average maternal weight may be lower average survival rates of their offspring as first-year survival in ungulates is correlated to weight (Gaillard et al., 1997b; Linnell et al., 1998; Loison et al., 1999). This provides a proximal mechanism explaining why juvenile survival rate is one of the first demographic parameters to decrease when environmental conditions worsen, a pattern pervasively found among large mammals (Eberhardt, 1985; Gaillard et al., 2000b).
A second subtle mechanism may have reinforced the negative effect of low average female body weight on the survival of their offspring. Indeed, females lost weight more quickly during the year with light female phenotypes. This may have some indirect and delayed consequences on neonatal survival by decreasing the ability of females to produce enough milk. Indeed, reindeer females rely on fat reserves for producing milk during early stages of lactation (Skogland, 1990). Such species relying on reserves for reproduction have been categorized as "capital breeder," as opposed to "income breeder" species, which use only energy acquired during the reproductive period for reproduction (Jönsson, 1997; Stearns, 1992). For species with a capital breeding strategy, the problem of relative resource allocation to maintenance or reproduction becomes complex and has to be addressed at multiple time scales (Bonnet et al., 1999; Jönsson, 1997) because resource acquisition and fat use may be delayed in time. If stored fat is used during winter for maintenance and gestation, which is less costly than lactation (Oftedal, 1985; Clutton-Brock et al., 1989), little energy would remain for females to satisfy the high energetic demands of neonates (Oftedal, 1985). Therefore, two mechanisms may act in synergy to explain a decreased juvenile survival of offspring when females were light: an immediate effect due to low birth weight and a possible delayed effect of early weight loss acting during the lactation period. The variation in body weight, most probably due to density dependence, associated with the lack of variation in resource allocation to reproduction is likely to produce a cascade effect, which directly impacts individual fitness and population dynamics.
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ACKNOWLEDGEMENTS |
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We thank D. Allainé, J. M. Gaillard, Ø. Holland, J. Linnell, A. Mysterud, E. J. Solberg, and T. Tveraa, who provided useful comments on earlier drafts of this manuscript. We also greatly benefited from comments by D. Westneat, R. Weladji, and an anonymous referee.
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REFERENCES |
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